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RESEARCH ARTICLE

Game-based learning environments affect frontal brain activity

Silvia Erika KoberID1,2*, Guilherme WoodID1,2, Kristian Kiili3, Korbinian Moeller4,5,6, Manuel NinausID4,5

1 Institute of Psychology, University of Graz, Graz, Austria, 2 BioTechMed-Graz, Graz, Austria, 3 Faculty of Education and Culture, Tampere University, Tampere, Finland, 4 Centre for Mathematical Cognition, School of Science, Loughborough University, Loughborough, United Kingdom, 5 Leibniz-Institut fu¨r Wissensmedien, Tu¨bingen, Germany, 6 LEAD Graduate School & Research Network, Eberhard-Karls University Tu¨bingen, Tu¨bingen, Germany

*silvia.kober@uni-graz.at

Abstract

Inclusion of game elements in learning environments to increase motivation and learning outcome is becoming increasingly popular. However, underlying mechanisms of game- based learning have not been studied sufficiently yet. In the present study, we investigated effects of game-based learning environments on a neurofunctional level. In particular, 59 healthy adults completed a game-based version (including game elements such as a narra- tive and virtual incentives) as well as a non-game-based version of a number line estimation task, to improve fractional knowledge, while their brain activity was monitored using near- infrared spectroscopy. Behavioral performance was comparable across the two versions, although there was a tendency that less errors were made in the game-based version. How- ever, subjective user experience differed significantly between versions. Participants rated the game-based version as more attractive, novel, and stimulating but less efficient than the non-game-based version. Additionally, positive affect was reported to be higher while engaging in the game-based as compared to the non-game-based task version. Corroborat- ing these user reports, we identified increased brain activation in areas associated with emo- tion and reward processing while playing the game-based version, which might be driven by rewarding elements of the game-based version. Moreover, frontal areas associated with attention were also more activated in the game-based version of the task. Hence, we observed converging evidence on a user experience and neurofunctional level indicating that the game-based version was more rewarding as well as emotionally and attentionally engaging. These results underscore the potential of game-based learning environments to promote more efficient learning by means of attention and reward up-tuning.

Introduction

In recent years, game elements have been incorporated into learning tasks in education with increasing frequency [1–3]. Game-based learning environments are assumed to increase inter- est, motivation, adherence to instructions, and, consequently, the learning outcome [2–4].

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Citation: Kober SE, Wood G, Kiili K, Moeller K, Ninaus M (2020) Game-based learning environments affect frontal brain activity. PLoS ONE 15(11): e0242573.https://doi.org/10.1371/

journal.pone.0242573

Editor: Peter G. Roma, NASA Johnson Space Center, UNITED STATES

Received: May 28, 2020 Accepted: November 4, 2020 Published: November 19, 2020

Copyright:©2020 Kober et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability Statement: Data are available from the authors after contacting the Ethics Committee of the University of Graz

(ethikkommission@uni-graz.at) for researchers who meet the criteria for access to confidential data. These ethical restrictions prohibit the authors from making the minimal data set publicly available. When the Ethics Committee of the University of Graz agrees, the readers can contact Silvia Erika Kober (silvia.kober@uni-graz.at) to request the data. With an approval of the Ethics Committee of the University of Graz, we confirm

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Game elements may include game mechanics (e.g., core activities repeated by the learner throughout the game), visual aesthetics, narrative of a game (storyline), incentives such as scores (points), stars, badges, trophies, power-ups, or any other rewards, or sounds [5]. Gener- ally, games or game elements are assumed to be rewarding [2,6–11]. For instance, King et al.

(2011) [12] found that game elements such as incentives (earning points) were rated as the most enjoyable and important aspects of video game playing. Moreover, providing concise, real-time feedback of actual performance by means of game elements such as rewards was found to lead to stronger engagement of the learner [5,9,13,14]. As such, there is already evi- dence that game-based learning environments lead to improved learning outcomes compared to conventional educational approaches [3,4]. However, there is also consensus that more studies in terms of large randomized control trials are necessary to better understand underly- ing working mechanisms in game-based learning tasks and to draw a meaningful conclusion [2,3]. Although the number of studies investigating behavioral effects of game-based learning is increasing, effects of game-based learning environments on brain activation patterns, which are associated with learning processes, are investigated only scarcely still.

In this context, we investigated neuronal correlates of playing a game-based and a non-game- based version of a number line estimation task which requires participants to indicate the correct location of a given target number on a number line of which only start and endpoint are given.

Importantly, this task was found to assess and train number magnitude understanding [15,16].

The game-based and non-game-based number line estimation solutions of the current study were developed with theSemideusresearch engine which allows for customization of game elements and was originally developed to improve conceptual fractional knowledge in children [17]. In both versions, participants performed the number line estimation task, in which they had to indi- cate the position of fractions (e.g., 3/7) on a horizontal line ranging from 0 to 1. In contrast to the non-game-based version, the game-based version included game elements such as a narrative and virtual incentives. Positive/negative feedback was presented in both task versions.

Behavioral studies showed that game-based versions of the number line estimation task can be used to effectively train and assess fractional knowledge in children [17–20]. To examine whether the inclusion of game elements affects brain activation patterns when performing the number line estimation task, we used near-infrared spectroscopy (NIRS). NIRS measures changes in the hemodynamic response (relative concentration changes of oxygenated and deoxygenated hemoglobin in the outer layer of the cortex; oxy- and deoxy-Hb) of the brain.

Generally, neuronal activation in specific brain areas leads to a localized vascular response that causes an influx of oxygen-rich blood to the active area and its surrounding tissue. Conse- quently, this leads to an increase in oxy-Hb and a decrease in deoxy-Hb in active brain regions [21]. NIRS is a non-invasive, portable, easy-to-use, and inexpensive neurofunctional method that does not restrict participants’ movements or natural behavior while performing a task as compared to other methods (e.g. the electroencephalogram -EEG- or functional magnetic res- onance imaging -fMRI-) [22].

The majority of studies investigating neuronal correlates of gaming used EEG or fMRI.

According to a review article by Palaus et al. (2017), 8 studies used NIRS to investigate neuronal correlates of gaming. In these NIRS studies, different types of games were used such as action games, ego-shooters, puzzle games, strategy games, rule learning games, or racing games [10].

Therefore, reported changes in brain activity due to gaming were rather heterogeneous. Some studies reported a global decrease of oxy-Hb over frontal brain areas during gaming [23–27].

However, differences in task complexity, cognitive load, expertise, or subjective user experience during playing may have added to these different brain activation patterns [28–32].

Effects of game-based learning environments on brain activation patterns have hardly been investigated so far. In a pilot study, Baker et al. (2015) investigated neuronal correlates during

that data will be available upon request to all interested researchers.

Funding: MN was supported by the Leibniz- Competition Fund (SAW-2016-IWM-3) and the Leibniz-WissenschaftsCampus “Cognitive Interfaces” (MWK-WCT TP12). The authors acknowledge the financial support by the University of Graz. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

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playing a computer-based fraction learning game calledRefractionusing NIRS. Refraction requires the player to combine math (i.e., fractions) and spatial (i.e., screen navigation) skills to complete a series of game stages successfully. Beside the combined math and spatial tasks, the authors also added two control conditions in which participants either performed only math or spatial tasks. They found stronger activation within parietal and prefrontal brain regions when participants performed the combined tasks in the game Refraction compared to solely spatial activities or math tasks. They interpreted the observed increased activation over prefrontal areas when playing Refraction as a sign of increased working memory load and attentional demands when playing the game Refraction [33].

In the present study, our primary aim was to investigate a larger sample of adults and directly compare brain activation patterns associated with playing a game-based (including game elements) and a content-wise equivalent non-game-based version [17]. Game elements are assumed to increase engagement in the task, positive affect, motivation, and consequently the learning outcome [5,10,11,14]. In particular, there is empirical evidence that such game elements can activate the reward system in the brain [6,10,34–38]. On a general level, previ- ous fMRI studies showed that reward and emotion processing can increase prefrontal brain activation, which was associated with working memory and attention [36,39–45] [for general reviews on prefrontal function and location see46,47]. Furthermore, previous fMRI studies indicated that spatial-numerical tasks in general [48–50] and the number line estimation task in particular [51], lead to neuronal activation in a fronto-parietal brain network. Therefore, we also focused specifically on changes in brain activation patterns over prefrontal areas during gaming. As in the current study, task content and complexity were held constant across the game-based and the non-game-based version, differences in brain activation patterns between versions should be related to the incorporation of game elements. We expected the game ele- ments to be rewarding and emotionally engaging [7,8,14] and thus to lead to stronger pre- frontal brain activation compared to the non-game-based version.

Beside our main research question concerning effects of a game-based learning environ- ment on brain activation patterns, we also investigated behavioral effects as secondary research question. Concerning task performance, there are heterogeneous results reported in the litera- ture. Some studies reported beneficial effects of game-based tasks on behavioral performance, other studies argued that game elements might induce cognitive overload and distract learners from the actual task [3–5,9,11,52–57]. Therefore, we also analyzed possible differences in task performance between the two versions.

In a tertiary and more exploratory research question, we focused on subjective user experience including flow and affective state, when performing both versions of the task. Prior studies showed that a game-based version of a task can lead to a stronger flow experience and higher user experience ratings than a non-game-based version of the same task [14,58–61]. Flow is defined as a positive emotional state of optimal performance [62]. Generally, flow experience seems posi- tively related with learning outcomes and playing performance in game-based learning

approaches [58–60,63,64] and was often associated with positive user experience [58,65]. How- ever, there are also studies that found no differences in flow experince between game-based and non-game-based versions of the same task [9]. Therefore, we also investigated the subjective user experience, flow, and affective state while playing both task versions in the present study.

Methods Participants

Fifty-nine right-handed healthy adults (29 female, 30 male, mean age = 22.85 yrs.,SD= 3.60;

all were Caucasian) took part in this study. Fifty-one were students, eight were employees

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(lawyers, medical doctors, software engineers). They had normal or corrected-to-normal vision. Participants were recruited via fliers and advertisements, personal recruitment, as well as via mailing lists of the University of Graz. They did not get any financial compensation. Psy- chology students got a partial course credit. Participants gave written informed consent prior to testing. The study was approved by the Ethics Committee of the University of Graz, Austria (reference number GZ. 39/86/63 ex 2017/18) and is in accordance with the ethical standards of the Declaration of Helsinki.

Task–game-based vs. non-game-based task

All participants performed a game-based and a non-game-based version of a number line esti- mation task. Half of the participants started with the game-based version, the other half with the non-game-based version. In the number line estimation task, participants had to locate a given target fraction (e.g., 3/7) on a number line ranging from 0 to 1. In each version (game- based vs. non-game-based) 48 fractions involving single- (e.g., 3/7) and double-digit (e.g., 19/

25) numerators and denominators were presented. The game-based version of the number line estimation task (seeFig 1A) was realized with the Semideus research game engine, which allows for easy inclusion of several game elements [17,19]. The non-game-based version of the number line estimation consisted of a stripped version of the task without any game elements (Fig 1B) but maintained positive/negative feedback. It corresponds to the conventional num- ber line estimation task [e.g.,15]. Both versions were comparable regarding task difficulty as they involved the same target fraction as well as number of levels (i.e., 6 levels, each including 8 tasks/fractions).

In both versions, a target fraction to-be-located on the number line was displayed in the upper left part of the screen. Participants could move a cursor (white bar in the non-game- based version) or the game character Semideus (in the game-based version) on the number line with the left and right arrow keys on a standard QWERTZ keyboard and confirm their estimates by pressing the space bar. Feedback was provided immediately after each estimation.

In the non-game-based version, positive feedback was given by showing a green check mark

Fig 1. Examples scenes of the game-based and non-game-based task version. Exemplary screenshots of the game-based version (A) and the non-game-based version (B) of the number line estimation task when receiving positive feedback after correct estimation.

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above the cursor in case the target fraction was estimated accurately (i.e., estimated location no more than±5% away from the correct location) and at the same time the absolute correct loca- tion was shown by a green marker on the number line. Negative feedback was given in the form of a red cross in case the estimated location was more than±5% away from the correct location. The same negative feedback mechanic was shown when the estimation took too long (>10 seconds).

In the game-based version, positive feedback was provided through gestures of Semideus (e.g. lifting hands up and cheering) when estimations were correct (i.e., estimated location no more than±5% away from the correct location). Additionally, participants earned virtual coins for accurate estimations (i.e., over 98% = 500 coins; 97%–98% = 300 coins; 96%–95% = 100 coins). For inaccurate estimates (i.e., estimates more than±5% away from the correct loca- tion) the game character Semideus was struck by lightning and the player lost 10 units of vir- tual energy (displayed by an orange bar on the right side of the screen, seeFig 1A) on the first error in a trial, 5 units of energy for the second error on the same trial, and 2.5 units of energy for any further error on that same trial/item. The same negative feedback mechanic (loss of energy and lightning) was used when players took too long to make their estimation (i.e., pressing the space bar,>10 seconds). This time limit was visualized by a cloud getting darker with passing time and a numerical countdown within the cloud.

In general, the game-based version employed typical characteristics of games (Plass et al., 2015) such as narrative elements (story line: Semideus tries to find gold coins that a goblin has stolen from Zeus and hidden along the trails of Mount Olympus), appealing visual aesthetics, virtual incentives in the form of points and stars earned depending on the performance of par- ticipants, as well as positive/negative feedback. A comprehensive description of the game ele- ments used in the game-based version and the rational of using them can be found in Ninaus et al. (2019) [14].

The number of estimation attempts on each task was not limited and participants had to estimate the location of the fraction correctly before they were allowed to proceed to the next task. After correct estimations, participants were asked to press the Enter-key to proceed to the next task.

In both versions, the absolute number of errors, mean estimation accuracy, and mean dura- tion per task/fraction were used as dependent variables for statistical analysis.

NIRS-recordings and -analysis

To measure relative concentration changes of oxygenated (oxy-Hb) and deoxygenated hemoglo- bin (deoxy-Hb) over frontal areas during the game-based and non-game-based version of the line estimation task, measurements were performed on a continuous wave system (ETG-4000, Hitachi Medical Co., Japan) using two 3x5 optode probe sets (consisting of 7 photo-detectors and 8 light emitters) resulting in a total of 22 channels (seeFig 2). The ETG-4000 uses two different wave- lengths (695±20 nm and 830±20 nm). Distance between optodes was 3 cm when mounted. Sam- pling rate of the NIRS system was set to 10 Hz. Channel configuration of the NIRS probe set is given inFig 2. It was positioned over the forehead. In accordance with the international 10–20 placement system, we used Fz (emitter 7) as marker position to place the probe set. The 22 NIRS channels were merged to regions of interest (ROI) for statistical analysis (Fig 2B).

The MNI coordinates of the NIRS channels were determined using AtlasViewer [66]. In Table 1, the anatomic labels are listed for each NIRS channel.

For offline analyses of the NIRS signal, we investigated changes in oxy-Hb and deoxy-Hb separately using the Homer2 NIRS Processing package [67] based on MATLAB (Mathworks, MA USA). The following NIRS signal processing steps were performed [68]:

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The raw optical intensity data series were converted into changes in optical density (OD).

Channels with very low optical intensity where discarded from the analysis using the function enPruneChannels. Then an automatic motion correction was applied using a wavelet trans- form method (function hmrMotionCorrectWavelet, iqr = 0.1) [69]. Additionally, artifacts, which were still in the signal were identified (function hmrMotionArtifact, signal change greater than std_threshold of 10 or amp_treshold of 5). The signal was filtered with a low-pass filter of 0.5 Hz. Then optical density data were converted into concentration changes (function hmrOD2Conc, ppf = 6.0 6.0). Marked artifacts were rejected (tRange -10 to 10 seconds).

The time courses of oxy-Hb and deoxy-Hb (hemodynamic response) of the remaining lev- els were averaged task-related separately for both versions (game-based and non-game-based version, average across 6 levels each) in each individual separately. Task-related concentration changes of oxy-Hb and deoxy-Hb were referred to a 5s baseline interval prior to level onset (seconds -5 to 0). For statistical analyses, oxy-Hb and deoxy-Hb was averaged for the time period during the task (0–50 s after level onset).

Questionnaires

To assess subjective experience of participants, they had to fill in the Flow Short Scale (FKS) [70], the User Experience Questionnaire (UEQ) [71], and the German version of the Positive and Negative Affect Schedule (PANAS) [72] once after the game-based and the non-game- based version of the number line estimation task each.

Fig 2. Position of the optode probe set on the head of participants. (A) Placement of the 22 NIRS channels on the forehead. (B) Positions of the nine regions of interests (ROIs). (C) Channel configuration and positions of the emitters (red circles) and detectors (blue circles) of the optode probe set (3x5). Numbers in the white rectangles represent the respective NIRS channel number.

https://doi.org/10.1371/journal.pone.0242573.g002

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The Flow Short Scale (FKS) [70] assesses flow experience using 10 items. Six of the items measure “fluency of performance” (e.g., “I have no difficulty concentrating”) and four items measure “absorption by activity” (e.g., “I don’t notice time passing”) on a 7-point scale (1

=“not at all” - 7 = “very much”). Additionally, 3 items measure perceived importance or per- ceived outcome importance (concern, e.g., “I must not make any mistakes here”) and 3 further items assess demand, skills, and the perceived fit of demands and skills (e.g., “Compared to all other activities which I partake in, this one is. . .”–answers are possible on a 9-point scale rang- ing from 1 =“easy” to 9 =“difficult”). The mean of each component was used as dependent var- iable in the analyses.

The User Experience Questionnaire (UEQ) is generally used to assess interaction quality of certain design variations of (software) products and whether these catch the user’s attention and interest [73]. Accordingly, this questionnaire assesses conventional usability aspects or (goal-directed) pragmatic quality (efficiency, transparency/perspicuity, controllability/depend- ability), user experience or (non-goal-directed) hedonic quality (novelty, stimulation), as well as attractiveness by using bipolar ratings, such as “unpleasant—pleasant” or “appealing–repel- ling”. The subscaleattractivenessdescribes the overall impression of the task, whether partici- pants like or dislike it.Transparency/perspicuitydescribes the easiness to get familiar with the task and to learn how to use it.Controllability/dependabilityis related to the users’ feeling of control of the interaction and whether it is secure and predictable. The subscaleefficiency reflects whether the user can solve the tasks without unnecessary effort and whether it reacts fast.Noveltydescribes whether participants find the design of the task creative and whether it catches their interest. The subscalestimulationreflects whether the task is exciting and

Table 1. Anatomic labeling of NIRS channel positions (MNI coordinates) and merged regions of interests (ROI).

Ch nr. Emitter Detector Label name Ch coord. MNI

ROI1 1 1 1 Orbitofrontal cortex left -29 64–2

2 2 1 -11 64 0

ROI2 3 2 2 Orbitofrontal cortex right 15 70–2

4 3 2 26 51 2

ROI3 5 1 3 Middle frontal cortex left -42 61 4

10 4 3 -19 50 8

14 6 3 Inferior frontal cortex left -29 41 16

ROI4 6 4 1 Superior frontal cortex left -14 52 4

15 4 6 -10 45 20

ROI5 7 2 4 Medial superior frontal cortex 0 55 14

11 4 4 -9 69 23

12 5 4 12 51 18

16 7 4 2 50 32

ROI6 8 5 2 Superior frontal cortex right 19 52 4

17 5 7 21 57 28

ROI7 9 3 5 Middle frontal cortex right 37 48 2

13 5 5 21 46 10

18 8 5 Inferior frontal cortex right 37 40 18

ROI8 19 6 6 Middle frontal cortex left -14 39 26

20 7 6 Superior frontal cortex left -8 55 44

ROI9 21 7 7 Superior frontal cortex right 13 55 48

22 8 7 Middle frontal cortex right 22 41 30

Ch: Channel; MNI: Montreal Neurological Institute; ROI: Region of interest.

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motivating and whether it is fun to use. Transformed values range from -3 to +3, where +3 rep- resents the most positive and the -3 the most negative value [74].

To measure affective responses (mood and emotion), we used the German version of the Positive and Negative Affect Schedule (PANAS) [72]. The PANAS comprises 20 items, with 10 items measuring positive affect (e.g., excited, inspired) and 10 items measuring negative affect (e.g., upset, afraid). Each item is rated on a five-point scale, ranging from 1 = “Not at all” to 5 =

“Extremely”, to measure the extent to which the respective affect has been experienced in a spec- ified time frame. The items can be split up to four subscales: Joy, activity/interest, afraid, upset.

Procedure

Participants were tested individually. After providing informed consent and reading the instructions, NIRS optodes were mounted on their heads and quality of the NIRS signals being recorded was checked. Then, half of the participants started with the game-based version and the other half started with the non-game-based version of the number line estimation task.

Counterbalancing of the task versions was done in a pseudo-randomized order so that the same number of male and female participants started with the same task version. Before each task, one practice trial (1 level including 8 tasks) had to be performed. After completing the first version (6 levels, each including 8 tasks), participants completed the FKS, UEQ, and PANAS questionnaires to assess their subjective experience during the previously completed task. Then, the second version had to be performed before completing the FKS, UEQ, and PANAS questionnaires again. Overall, the experiment took about one hour.

Statistical analysis

To identify NIRS channels that showed the strongest NIRS signal change (oxy- and deoxy-Hb) due to the game-based vs. non-game-based version (average of second 0 to 50 after level onset), we used the False Discovery Rate (FDR) method to control the proportion of false posi- tives among the channels that are detected as significant [75]. Therefore, one samplet-tests against 0 were calculated per channel and version to reveal whether relative NIRS signal changes differ from 0. Significant differences from 0 in oxy- and deoxy-Hb were then deter- mined by using the FDR method.

To compare NIRS signal change between the game-based and non-game-based task version statistically, analyses of variances (ANOVAs) for repeated measures were applied including the within-subject factorsTASK-VERSION(game-based vs. non-game-based version) and HEMISPHERE(left vs. right), separately for oxy- and deoxy-Hb. In particular, separate ANO- VAs for different regions of interest (ROIs) were performed. Therefore, the 22 NIRS channels were merged to 9 ROIs (ROI1: channels 1 & 2; ROI2: channels 3 & 4; ROI3: channels 5, 10, and 14; ROI4: channels 6 & 15; ROI5: channels 7, 11, 12, and 16; ROI6: channels 8 & 17; ROI7:

channels 9, 13, and 18; ROI8: channels 19 & 20; ROI9: channels 21 & 22; see alsoTable 1and Fig 2). One ANOVA was performed for ROIs over the left vs. right orbitofrontal cortex (ROI 1 vs. ROI 2), one ANOVA was performed for ROIs over the left vs. right middle and inferior frontal cortex (ROI 3 vs. ROI 7), one for ROIs over the left vs. right superior frontal cortex (ROI 4 vs. ROI 6), one for ROIs over the left vs. right middle/superior frontal cortex (ROI 8 vs.

ROI 9), and one ANOVA with the within-subject factorTASK-VERSIONover the medial superior frontal cortex (ROI 5).

To test performance differences in the number line estimation task, we ran pairedt-tests on error rate, mean estimation accuracy, and mean duration per task comparing game-based and non-game-based version. To evaluate differences between game-based and non-game-based version in the questionnaire data, we also ran paired samplet-tests.

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For statistical analyses, the probability of a Type I error was maintained at 0.05. For the pairedt-tests and multiple ANOVAs, Bonferroni-Holm corrections for multiple comparisons were applied [76]. To detect outliers, data were z-transformed per version. Values larger or smaller +/- 3 SD were rejected from statistical analysis (7% of NIRS data).

Results

NIRS-signal: Topographical distribution

As illustrated inTable 2, oxy-Hb significantly increased over channels 5, 8, and 17 for the game-based version, whereas no significant increase or decrease could be observed for the non-game-based version. Deoxy-Hb significantly decreased over 15 of the recorded 22 chan- nels in the game-based version. In the non- game-based version, deoxy-Hb significantly decreased over channel 13, but increased over channel 5. The topographical distribution of oxy- and deoxy-Hb per version is depicted inFig 3.

NIRS-signal: Game-based vs. non-game-based task

To analyze differences in brain activation patterns between the game-based and the non- game-based task version, different ANOVAs with the within-subject factorsTASK-VERSION andHEMISPHERE(left vs. right) were calculated separately for oxy- and deoxy-Hb.Fig 4

Table 2. Results of topographical analysis after FDR correction.

Oxy-Hb Game-based task Oxy-Hb Non-game-based task Deoxy-Hb Game-based task Deoxy-Hb Non-game-based task

Ch. Nr. p-value Ch. Nr. p-value Ch. Nr. p-value Ch. Nr. p-value Criticalp-value FDR

Ch5 8.98E-05 Ch7 0.0289 Ch13 2.27E-05 Ch13 1.38E-05 0.0045

Ch17 0.0037 Ch6 0.0529 Ch4 3.8E-05 Ch5 0.0020 0.0091

Ch8 0.0109 Ch19 0.0673 Ch12 5.53E-05 Ch17 0.0362 0.0136

Ch22 0.0221 Ch13 0.0757 Ch18 0.0001 Ch18 0.0400 0.0182

Ch14 0.0227 Ch4 0.0899 Ch11 0.0006 Ch8 0.0410 0.0227

Ch18 0.0254 Ch8 0.1160 Ch19 0.0006 Ch4 0.0826 0.0273

Ch9 0.0268 Ch10 0.1347 Ch10 0.0007 Ch14 0.0884 0.0318

Ch21 0.0480 Ch3 0.1765 Ch14 0.0008 Ch22 0.1059 0.0364

Ch15 0.0700 Ch15 0.1950 Ch21 0.0013 Ch19 0.1147 0.0409

Ch7 0.0734 Ch12 0.2103 Ch3 0.0025 Ch6 0.1187 0.0455

Ch6 0.1037 Ch5 0.2982 Ch1 0.0033 Ch7 0.1223 0.0500

Ch11 0.1152 Ch20 0.4103 Ch20 0.0044 Ch12 0.1293 0.0545

Ch12 0.1280 Ch18 0.4513 Ch22 0.0085 Ch21 0.1486 0.0591

Ch16 0.2110 Ch2 0.4587 Ch15 0.0136 Ch10 0.2168 0.0636

Ch13 0.2147 Ch21 0.4714 Ch17 0.0247 Ch15 0.2239 0.0682

Ch20 0.2354 Ch16 0.5124 Ch16 0.1215 Ch16 0.3460 0.0727

Ch10 0.2526 Ch22 0.7056 Ch8 0.1672 Ch9 0.4599 0.0773

Ch3 0.5623 Ch1 0.7432 Ch9 0.2064 Ch11 0.4793 0.0818

Ch4 0.6094 Ch14 0.8166 Ch6 0.3190 Ch1 0.5635 0.0864

Ch19 0.7074 Ch11 0.9463 Ch5 0.3276 Ch20 0.5974 0.0909

Ch1 0.7613 Ch17 0.9957 Ch2 0.8083 Ch3 0.6601 0.0955

Ch2 0.8987 Ch9 0.9968 Ch7 0.9686 Ch2 0.7786 0.1000

p-values of the one samplet-tests again 0 are listed in ascending order per channel and task version (game-based vs. non-game-based version), presented separately for oxy- and deoxy-Hb values. Additionally, criticalp-values as determined by the FDR correction are shown. Significant results are marked with asterisks. Ch: Channel;

FDR: False discovery rate.

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illustrates mean oxy-Hb values for each ROI and task version. InFig 5, mean deoxy-Hb values per ROI and task are shown.

Oxy-Hb orbitofrontal cortex (ROI 1 vs. ROI 2): The ANOVA revealed no significant results.

Oxy-Hb middle and inferior frontal cortex (ROI 3 vs. ROI 7): The main effectTASK-VER- SION(F(1,58) = 10.90,p<0.01,ηp2= 0.18) was significant. Activation was stronger in the game-based than in the non-game-based version (Fig 4).

Fig 3. NIRS topography. Topographical distribution of oxy- and deoxy-Hb during the game-based and non-game-based version.

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Fig 4. ANOVA results for oxy-Hb. Means andSEof oxy-Hb in the 9 regions of interests (ROI), presented separately for the game-based and non-game-based version. ROI 1: left orbitofrontal cortex; ROI 2: right orbitofrontal cortex;

ROI 3: left middle/inferior frontal cortex; ROI 4: left superior frontal cortex; ROI 5: medial superior frontal cortex; ROI 6: right superior frontal cortex; ROI 7: right middle/inferior frontal cortex; ROI 8: left middle/superior frontal cortex;

ROI 9: right middle/superior frontal cortex.

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Oxy-Hb superior frontal cortex (ROI 4 vs. ROI 6): The main effectTASK-VERSION(F (1,58) = 8.51,p<0.01,ηp2= 0.14) was significant indicating that activation was stronger in the game-based than in the non-game-based version (Fig 4).

Oxy-Hb middle/superior frontal cortex (ROI 8 vs. ROI 9): The interaction effectTASK-- VERSIONHEMISPHEREwas significant (F(1,58) = 8.40,p<0.01,ηp2= 0.14). The game-based version led to a stronger oxy-Hb increase than the non-game-based version over the right hemisphere (ROI 9), whereas no differences were observed over the left hemisphere (ROI 8, Fig 4).

Oxy-Hb medial superior frontal cortex (ROI 5): The ANOVA revealed no significant results.

Deoxy-Hb orbitofrontal cortex (ROI 1 vs. ROI 2): The main effectTASK-VERSION(F (1,58) = 5.36,p<0.05,ηp2= 0.10) was significant. Deoxy-Hb showed a stronger decrease in the game-based than in the non-game-based version (Fig 5). However, this effect was not signifi- cant any more after Bonferroni-Holm correction. Additionally, the significant main effect HEMISPHERE(F(1,58) = 8.62,p<0.01,ηp2= 0.15) indicated that the deoxy-Hb decrease was stronger over the right (ROI 2) than over the left orbitofrontal cortex (ROI 1,Fig 5).

Deoxy-Hb middle and inferior frontal cortex (ROI 3 vs. ROI 7): The significant main effect HEMISPHERE(F(1,58) = 12.04,p<0.01,ηp2= 0.20) indicated that the deoxy-Hb decrease was stronger over the right (ROI 7) than over the left middle/inferior frontal cortex (ROI 3,Fig 5).

Deoxy-Hb superior frontal cortex (ROI 4 vs. ROI 6): The ANOVA revealed no significant results. The main effectTASK-VERSION(F(1,58) = 3.62,p= 0.06,ηp2= 0.07) only showed a trend that deoxy-Hb showed a stronger decrease during the game-based than during the non- game-based version (Fig 5).

Deoxy-Hb middle/superior frontal cortex (ROI 8 vs. ROI 9): The ANOVA revealed no sig- nificant results.

Deoxy-Hb medial superior frontal cortex (ROI 5): The decrease in deoxy-Hb was by trend (F(1,58) = 3.12,p= 0.08,ηp2= 0.06) more pronounced during the game-based than during the non-game-based version (Fig 5).

Fig 5. ANOVA results for deoxy-Hb. Means andSEof deoxy-Hb in the 9 regions of interests (ROI), presented separately for the game-based and non-game-based version. ROI 1: left orbitofrontal cortex; ROI 2: right orbitofrontal cortex; ROI 3: left middle/inferior frontal cortex; ROI 4: left superior frontal cortex; ROI 5: medial superior frontal cortex; ROI 6: right superior frontal cortex; ROI 7: right middle/inferior frontal cortex; ROI 8: left middle/superior frontal cortex; ROI 9: right middle/superior frontal cortex.

https://doi.org/10.1371/journal.pone.0242573.g005

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InFig 6, the NIRS times courses of oxy- and deoxy-Hb are presented, separately for each of the 9 ROIs.

Behavioral results and user experience

InTable 3, means andSEof behavioral and user experience data are summarized as well as results of the statistical comparison between the game-based and non-game-based task version.

In the game-based version, less errors were made than in the non-game-based version (Table 3), although this difference was statistically no longer significant after Bonferroni-Holm correction. Accuracy and mean duration per task were comparable between versions. Flow experience did not differ between task versions (Table 3). There was only a non-significant trend that the perceived importance to be successful is higher in the game-based than in the non-game-based version. Additionally, the perceived fit of demands and skills seems to be descriptively higher in the game-based than in the non-game-based version. Results of the UEQ revealed that participants rated the game-based version to be more attractive, novel, and stimulating than the non-game-based version (Table 3). In contrast, participants experienced the non-game-based version as more efficient than the game-based version (Table 3). Accord- ing to the results of the PANAS, participants experienced more joy during the game-based than during the non-game-based version (Table 3).

Fig 6. NIRS time courses. NIRS time course of oxy-Hb (upper panel) and deoxy-Hb (lower panel) during the game-based (left panel) and non-game-based (right panel) version, presented separately for each of the nine regions of interests (ROI). ROI 1: left orbitofrontal cortex; ROI 2: right orbitofrontal cortex; ROI 3: left middle/

inferior frontal cortex; ROI 4: left superior frontal cortex; ROI 5: medial superior frontal cortex; ROI 6: right superior frontal cortex; ROI 7: right middle/inferior frontal cortex; ROI 8: left middle/superior frontal cortex; ROI 9: right middle/superior frontal cortex.

https://doi.org/10.1371/journal.pone.0242573.g006

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Discussion

The primary aim of the present study was to investigate neuronal correlates of game-based learning by contrasting brain activation patterns while performing a game-based and a non- game-based version of a number line estimation task. We expected the game-based version to be more rewarding and emotionally engaging leading to a stronger activation in the prefrontal cortex. Possible differences in behavioral parameters such as task performance and user expe- rience including flow and affect were examined in secondary and tertiary research questions, too. Since prior studies reported on heterogenous results concerning the effects of game-based learning tasks on user performance and experience, we did not formulate directed hypotheses in this context.

Brain activation

Concerning our main research question, we found stronger activation of prefrontal brain areas when participants performed the game-based as compared to the non-game-based ver- sion. Generally, prior fMRI studies showed that a network of fronto-parietal brain areas seems to be involved in number line estimation including the superior and middle frontal gyrus and dorsolateral prefrontal cortex [51]. However, while the role of parietal areas in number pro- cessing is well established [i.e., subserving actual processing of number magnitude informa- tion;77,78], the role of frontal areas is less well understood and often considered to reflect also non-numerical mechanisms such as attention [for a meta-analysis see79].

Prefrontal brain areas were also strongly activated in the present study, especially in the game-based version (relative increase in oxy-Hb and decrease in deoxy-Hb). Moreover, in a fMRI study by Vogel et al. (2013), number line estimation led to strong activation of bilateral prefrontal cortices, which was more pronounced for the right than on the left hemisphere in

Table 3. Behavioral and user experience data (means andSE) and results of the statistical comparison between the game-based and non-game-based task version.

Game-based task Non-game-based task

Mean(SE) Mean(SE) p-values oft-tests

Estimation performance Error rate 24.98 (1.69) 28.76 (1.97) 0.02

Mean Accuracy (%) 94.76 (0.20) 94.52 (0.21) 0.21

Mean duration per task (ms) 8109.07 (264.44) 7930.53 (266.13) 0.49

Flow Overall 4.50 (0.12) 4.43 (0.13) 0.49

Fluency 4.72 (0.14) 4.70 (0.15) 0.84

Absorption 4.18 (1.10) 4.04 (0.16) 0.35

Perceived importance 2.24 (0.14) 1.96 (0.14) 0.04

Perceived fit of demands and skills 4.18 (0.15) 3.99 (0.16) 0.05

User experience Attractiveness 0.98 (0.12) 0.07 (0.15) <0.001

Efficiency 1.04 (0.09) 1.30 (0.10) 0.007

Transparency/Perspicuity 1.95 (0.10) 2.12 (0.10) 0.11

Controllability/Dependability 0.97 (0.11) 1.11 (0.10) 0.21

Novelty 0.64 (0.15) -0.78 (0.18) <0.001

Stimulation 0.53 (0.16) -0.09 (0.17) 0.002

Positive/ negative affect Joy 2.51 (0.09) 2.30 (0.09) 0.01

Activity/ Interest 3.35 (0.08) 3.25 (0.10) 0.24

Afraid 1.29 (0.04) 1.26 (0.03) 0.32

Upset 1.27 (0.38) 1.17 (0.29) 0.07

Significant results are marked with asterisks.

https://doi.org/10.1371/journal.pone.0242573.t003

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the superior and middle frontal gyrus. Results of the present study also indicate that activation patterns were bilaterally distributed, but in some ROIs, with stronger signal changes observed over the right hemisphere than over the left hemisphere. For instance, deoxy-Hb showed a stronger decrease over the right orbitofrontal cortex and middle and inferior frontal cortex than over the left orbitofrontal cortex and middle and inferior frontal cortex. However, analy- sis of activation changes over single channels revealed also strong activation patterns over the left hemisphere, such as a strong increase in oxy-Hb over the left inferior / middle frontal cor- tex. Generally, these results are well in line with the findings by Vogel et al. (2013). In sum- mary, brain activation patterns observed are comparable with previous neuroimaging evidence on the neuronal correlates of number line estimation. These prefrontal brain activa- tion patterns (increase in oxy- and decrease in deoxy-Hb) were more pronounced for the game-based as compared to the non-game-based version and might indicate that participants paid more attention in the game-based version [79].

Moreover, the game-based version might have been more rewarding than the non-game- based version leading to increased attention towards the more rewarding environment and associated stronger prefrontal activation in turn. Playing computer games was observed to be able to activate the reward system of the brain [6,10,34–38]. Neuroimaging studies reported a positive association between increased prefrontal brain activity and reward processing [36, 39–43]. For instance, the orbitofrontal cortex (together with anterior cingulate cortex, ACC) was argued to be involved in providing a motivational value of cue-inducing stimuli [6,80].

Activation in the orbitofrontal cortex was found to decrease in the absence of an expected reward [6,10]. The game elements included in the game-based version, such as the more pro- nounced positive feedback for successful performance (earning reward points, gestures of the game character, etc.), are assumed to be rewarding [7,8]. This is backed by subjective ratings of the participants that also indicated the game-based version to be experienced as more rewarding than the non-game-based version. Hence, game elements might have led to stronger reward processing, which was associated with prefrontal brain activation, previously.

Another explanation for the stronger prefrontal activation in the game-based as compared to the non-game-based version might be that the emotional appeal was stronger in the game- based than in the non-game-based version [5]. In particular, we found increased activation (stronger decrease in deoxy-Hb) in the orbitofrontal cortex which is–amongst other areas–

involved in emotion regulation and reliably activated by feelings of pleasure [for a review see 44]. In fact, recent studies indicated that game elements may well influence emotional states [5, 14,81,82]. Our neurofunctional results are in line with this idea, which is further corroborated by participants’ subjective ratings with positive affect (joy) rated higher in the game-based as compared to the non-game-based version. Generally, it was observed that emotional processing, whether positive or negative, lead to increased activation in prefrontal brain regions [83–85].

This indicates that the increased prefrontal activation in the game-based version might be caused by increased emotional processing or emotional engagement in the gaming task.

Moreover, previous neurofunctional studies found increased frontal brain activation during game-based task versions with higher flow experience [28,32,86]. Using NIRS, de Sampaio Barros et al. (2018) investigated neuronal correlates of flow experience during gaming. They found that oxy-Hb was highest in an optimal state of task demands experienced to balance player resources. In the present study, we also found higher levels of oxy-Hb in the game- based version, for which participants reported that their perceived fit of demands and skills was higher (although statistically not significant) than in the non-game-based version. How- ever, as we did not find any statistically significant differences in the subjective flow experience between task versions, differences in flow experience may not explain the differences in pre- frontal activation.

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Differences in task difficulty or cognitive load [10,29,31,33,87–89] can also not explain differences in prefrontal activation patterns between the two task versions because task diffi- culty was comparable between the game-based and non-game-based version of the present study (with even a trend towards better performance in the game-based version as reflected in errors committed). However, although differences in game elements between the two versions did not lead to significant differences in behavioral performance, one cannot exclude that the need of processing the richer input (i.e., added game elements) in the game-based version led to increased frontal activation [90].

Behavioral performance

Behavioral performance was comparable between the two task versions. Although participants made fewer errors in the game-based as compared to the non-game-based version, this differ- ence in behavioral performance was statistically no longer significant after controlling for mul- tiple comparisons. The observed comparable behavioral performance in both task versions shows on the one hand, that game elements did not interfere with participants’ task perfor- mance, as suggested by literature on seductive details [55–57]. In turn, this might indicate that game elements were integrated in a coherent and meaningful way and connected to the task [55,91]. On the other hand, adding game elements to a learning task–here to the number line estimation task–did not lead to a statistically significant performance improvement as found in previous studies [for a meta-analysis see4].

However, it has to be noted that the majority of previous studies used interventions, in which participants performed the game-based learning task over repeated and/or longer train- ing sessions. In the present study, we acquired neurofunctional data and therefore participants completed only one session. Hence, one may not assume that fraction knowledge was fostered significantly within this single session. Moreover, the estimation accuracy of the participants was already high and thus clear improvements were not even expected. Taken together, our results indicate that adding game elements to a number line estimation task had neither signif- icant beneficial nor negative effects on task performance within one session.

User experience, affect, and flow

In contrast to behavioral performance, subjective user experience differed significantly between task versions. Participants rated the game-based version as more attractive, novel, and stimulating than the non-game-based version. Hence, they seemed to like the game-based ver- sion more than the non-game-based version (subscale attractiveness), experienced the game- based version as more exciting and motivating (subscale stimulation), and found the game- based version more creative, so that it caught their interest more than the non-game-based ver- sion (subscale novelty) [74]. Additionally, positive affect was higher during the game-based than the non-game-based task. This is in line with prior findings. For instance, Heidig et al.

(2015) found that the perceived aesthetics of a game learning task positively affects the emo- tional states of the learners. While the emotional states had a minor impact on learning out- comes, they had a larger impact on intrinsic motivation, including motivation to continue working with the material [81]. Kiili, Lindstedt, and Ninaus (2018) also found that intrinsically motivated students showed higher positive affect when playing Semideus over a longer time period [61]. In a similar study, Ninaus et al. (2019) [14] found overall increased emotional engagement in a game-based compared to a non-game-based version of a number line estima- tion task utilizing both conventional paper-pencil questionnaires as well as automatic facial emotion detection. Hence, adding game elements to the task increased the attractiveness of the task and increased positive affect, which might positively affect motivation and the time

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learners spent with the learning environment. However, it has been suggested, that beneficial aspects of game elements require careful balancing of emotional features as these features might also overstrain individual’s emotional regulation capabilities [92,93].

Furthermore, it needs to be mentioned that even though participants rated the game-based version as attractive, novel, and stimulating, they also rated the game-based version of the task as less efficient than the non-game-based version. However, this subjective user experience was not reflected by the behavioral performance because both task versions led to comparable performance in the number line estimation task.

We also assessed flow experience, because flow is one the most popular motivational con- structs assessed in gaming studies and suggested to positively affect learning outcomes [58].

We did not find any statistically significant differences in the flow experience between the two task versions. There was only a non-significant trend that the perceived importance to be suc- cessful was higher in the game-based than in the non-game-based version. Additionally, the perceived fit of demands and skills was descriptively higher in the game-based as compared to the non-game-based version. In a similar study, Ninaus et al. (2019) observed higher levels of flow in a game-based version compared to a non-game-based version of a number line estima- tion task [14]. However, the authors used a larger sample and thus were able to identify even smaller effects. Kiili and Ketamo (2018) [59] also found increased flow experience in a game- based number line estimation task when compared to its paper based non-game-based equiva- lent. Accordingly, not only game elements but also the medium (digital vs. paper-based) dif- fered between the two conditions, which makes a clear interpretation rather difficult. Future studies will need to further investigate the effects of game elements on flow experience.

Subjective flow experience is often associated with increased performance and learning gains, because flow constitutes a state of optimal balance between challenge and skill [60,63,64].

Probably, we did not find any differences in flow experience between task versions because of the lack of performance differences between the game-based and non-game-based version. That is, the game-based and non-game-based task versions were equally challenging. However, there are also prior studies that found significant performance differences between a game-based and a non-game-based task version but no differences in flow experience [9]. Interindividual differ- ences in flow experience might also contribute to the non-significant results [94,95].

Limitations

Performing only one fraction estimation session (7 minutes on average per task) was too short to reveal any significant differences in learning effects. Future studies investigating changes in neuronal correlates when performing this learning task over a longer time period comparing a game-based and a non-game-based task version are necessary to evaluate differential learning effects.

Concerning the increased frontal brain activation in the game-based task version, we can- not exclude that the need of processing the richer input (i.e., added game elements) in the game-based version led to a higher cognitive or mental workload and consequently to increased frontal activation patterns as already discussed before [90]. However, we did not observe significant differences in behavioral performance between the two task versions, which one might expect in case of high cognitive or mental workload due to the inclusion of game elements.

Conclusions and implications

The present study investigated neuronal correlates of adding game elements to a number line estimation task. We compared frontal activation patterns between a game-based and a non-

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game-based version of the same task. Additionally, possible differences in user performance and subjective user experience between task versions were investigated. Results showed that adding game elements to a learning task such as number line estimation lead to stronger acti- vation of brain areas, which were previously observed to be involved in a non-game-based number line estimation task.

Within one session we observed that prefrontal brain areas were activated more strongly in the game-based version, including game elements, as compared to the non-game-based ver- sion. This might reflect higher demands on reward and emotional processing as well as stron- ger attention towards the learning material when game elements are added. Hence, game- based learning tasks might also lead to a superior learning outcome in future training studies.

In particular, the association between neurofunctional activity in game-based learning and learning outcomes need to be investigated further.

In this context, adding game elements to traditional learning tasks used at school (e.g., ver- bal tasks, math tasks, natural science) might have beneficial effects, too. Additionally, game ele- ments might be used to design learning tasks, which have to be performed at home. Recently, the COVID-19 epidemic caused a school lockdown and a switch to digital learning. Many stu- dents were forced to perform their learning tasks at home with remote supervision of their teachers. This turned out to be challenging for students, teachers, as well as parents [96,97].

Here, using game-based learning environments might potentially improve home-based, digital learning outcomes and students’ motivation in the future. Summing up, results of the present study underscore the potential of game-based learning to promote more efficient learning by means of attention and reward up-tuning.

Author Contributions

Conceptualization: Silvia Erika Kober, Guilherme Wood, Kristian Kiili, Korbinian Moeller, Manuel Ninaus.

Data curation: Silvia Erika Kober.

Formal analysis: Silvia Erika Kober, Guilherme Wood, Manuel Ninaus.

Funding acquisition: Manuel Ninaus.

Investigation: Silvia Erika Kober, Manuel Ninaus.

Methodology: Silvia Erika Kober, Kristian Kiili, Korbinian Moeller, Manuel Ninaus.

Project administration: Silvia Erika Kober, Guilherme Wood.

Resources: Silvia Erika Kober, Guilherme Wood, Kristian Kiili, Manuel Ninaus.

Software: Silvia Erika Kober, Guilherme Wood, Kristian Kiili, Korbinian Moeller, Manuel Ninaus.

Supervision: Silvia Erika Kober, Guilherme Wood, Manuel Ninaus.

Validation: Silvia Erika Kober.

Visualization: Silvia Erika Kober.

Writing – original draft: Silvia Erika Kober, Manuel Ninaus.

Writing – review & editing: Silvia Erika Kober, Guilherme Wood, Kristian Kiili, Korbinian Moeller, Manuel Ninaus.

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